Plasma membrane/cell wall perturbation activates a novel cell cycle checkpoint during G1 in
            <i>Saccharomyces cerevisiae</i>

Kono, Keita; Al-Zain, Amr; Schroeder, Lea; Nakanishi, Makoto; Ikui, Amy E.

doi:10.1073/pnas.1523824113

Cited by 52 publications

(83 citation statements)

References 64 publications

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“…Conceptually, this trade-off suggests that the double mutant initially overshoots the optimum when nystatin concentrations are low, because the costs associated with each ergosterol mutation are combined (perhaps destabilizing the plasma membrane); by contrast, when nystatin concentrations are high, the optimum is shifted even farther away, and extreme reductions in ergosterol and potentially other sterols are needed for the yeast to survive, at which point the double mutant is most fit (see, e.g., Blanquart et al [42] for a theoretical exploration of this phenomenon). Because membrane damage can trigger cell cycle arrest in yeast [43], another possible explanation for the results observed at high concentrations of nystatin is that single mutants experience cell cycle arrest, reducing growth rate, whereas the additional stress caused by the combination of two mutations and high concentrations of nystatin may cause a checkpoint failure in double mutants, allowing the cells to bypass arrest and continue dividing (personal communication, C. Nislow to J. Ono).…”

Section: Discussionmentioning

confidence: 99%

Widespread Genetic Incompatibilities between First-Step Mutations during Parallel Adaptation of Saccharomyces cerevisiae to a Common Environment

2017

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Independently evolving populations may adapt to similar selection pressures via different genetic changes. The interactions between such changes, such as in a hybrid individual, can inform us about what course adaptation may follow and allow us to determine whether gene flow would be facilitated or hampered following secondary contact. We used Saccharomyces cerevisiae to measure the genetic interactions between first-step mutations that independently evolved in the same biosynthetic pathway following exposure to the fungicide nystatin. We found that genetic interactions are prevalent and predominantly negative, with the majority of mutations causing lower growth when combined in a double mutant than when alone as a single mutant (sign epistasis). The prevalence of sign epistasis is surprising given the small number of mutations tested and runs counter to expectations for mutations arising in a single biosynthetic pathway in the face of a simple selective pressure. Furthermore, in one third of pairwise interactions, the double mutant grew less well than either single mutant (reciprocal sign epistasis). The observation of reciprocal sign epistasis among these first adaptive mutations arising in the same genetic background indicates that partial postzygotic reproductive isolation could evolve rapidly between populations under similar selective pressures, even with only a single genetic change in each. The nature of the epistatic relationships was sensitive, however, to the level of drug stress in the assay conditions, as many double mutants became fitter than the single mutants at higher concentrations of nystatin. We discuss the implications of these results both for our understanding of epistatic interactions among beneficial mutations in the same biochemical pathway and for speciation.

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Section: Discussionmentioning

confidence: 99%

Widespread Genetic Incompatibilities between First-Step Mutations during Parallel Adaptation of Saccharomyces cerevisiae to a Common Environment

2017

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“…In Saccharomyces cerevisiae, the cell wall integrity (CWI) maintenance mechanism is intricately involved in this coordination (Levin, 2011). A dedicated checkpoint monitoring yeast CWI, regulates cell cycle progression depending on the state of the wall (Levin, 2011; Kono et al ., 2016).…”

Section: Introductionmentioning

confidence: 99%

Cellulose biosynthesis inhibition reduces cell cycle activity in a nitrate reductase- and cytokinin-dependent manner

Gigli-Bisceglia

Engelsdorf

Strnad

et al. 2018

Preprint

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During growth, development and defense, cell wall integrity needs to be coordinated with cell cycle activity. In Saccharomyces cerevisiae, coordination is mediated by the cell wall integrity maintenance mechanism. In plants, little is known how coordination is achieved.Here we investigated coordination between plant cell wall and cell cycle activity in Arabidopsis thaliana seedlings by studying the impact of cell wall damage (CWD, caused by cellulose biosynthesis inhibition) on cell cycle gene expression, growth, phytohormone (jasmonic acid, salicylic acid, cytokinins) and lignin accumulation.We found root growth and cell cycle gene expression are reduced by CWD in an osmosensitive manner. trans-zeatin application suppressed the CWD effect on gene expression.Quantification of cytokinins revealed CWD-induced, osmo-sensitive changes in several cytokinins. Expression of CYTOKININ OXIDASE2/DEHYDROGENASE (CKX2) and CKX3, encoding cytokinin-degrading enzymes, was elevated in CWD-exposed seedlings. Genetic studies implicated NITRATE REDUCTASE1/2 (NIA1/2) in the response to CWD. In nia1/2 seedlings CWD induced neither expression of CKX2/3 and cell cycle genes nor accumulation of jasmonic acid, salicylic acid and lignin.This suggests that CWD causes increased CKX2/3 expression through a NIA1/2-mediated process. Increased CKX expression seems to cause changes in cytokinin levels, leading to reduced cell cycle gene expression.

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“…More recently, it was also shown that a dedicated cell cycle checkpoint exists at the G1/S transition, which in response to plasma membrane and/or CWD inhibits cell cycle progression until the damage has been repaired (Fig. A) (Kono et al ).…”

Section: Regulation Of Cell Cycle Progression By the Ecm In Yeast Andmentioning

confidence: 99%

Outside‐in control – does plant cell wall integrity regulate cell cycle progression?

Gigli-Bisceglia

Hamann

2018

Physiologia Plantarum

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During recent years it has become accepted that plant cell walls are not inert objects surrounding all plant cells but are instead highly dynamic, plastic structures. They are involved in a large number of cell biological processes and contribute actively to plant growth, development and interaction with environment. Therefore, it is not surprising that cellular processes can control plant cell wall integrity (CWI) while, simultaneously, CWI can influence cellular processes. In yeast and animal cells such a bidirectional relationship also exists between the yeast/animal extracellular matrices and the cell cycle. In yeast, the CWI maintenance mechanism and a dedicated plasma membrane integrity checkpoint are mediating this relationship. Recent research has yielded insights into the mechanism controlling plant cell wall metabolism during cytokinesis. However, the knowledge regarding putative regulatory pathways controlling adaptive modifications in plant cell cycle activity in response to changes in the state of the plant cell wall are not yet identified. In this review, we summarize similarities and differences in regulatory mechanisms coordinating extracellular matrices and cell cycle activity in animal and yeast cells, discuss the available evidence supporting the existence of such a mechanism in plants and suggest that the plant CWI maintenance mechanism might also control cell cycle activity in plant cells.

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Plasma membrane/cell wall perturbation activates a novel cell cycle checkpoint during G1 in Saccharomyces cerevisiae

Cited by 52 publications

References 64 publications

Widespread Genetic Incompatibilities between First-Step Mutations during Parallel Adaptation of Saccharomyces cerevisiae to a Common Environment

Widespread Genetic Incompatibilities between First-Step Mutations during Parallel Adaptation of Saccharomyces cerevisiae to a Common Environment

Cellulose biosynthesis inhibition reduces cell cycle activity in a nitrate reductase- and cytokinin-dependent manner

Outside‐in control – does plant cell wall integrity regulate cell cycle progression?

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